Abstract
•Background: A previous study revealed the HNK-1 epitope in the human ciliary body beneath the ciliary epithelium. The molecules bearing this 3-sulphoglucuronic acid-containing oligosaccharide epitope in the eye remain unknown. As chondroitin sulphate proteoglycan (CSPG) and tenascin are potential candidates as bearers of the HNK-1 epitope, their distribution in the human eye was compared with that of the HNK-1 epitope. • Methods: Fifty-five formalin-fixed, paraffin-embedded human eyes, including 20 normal eyes and 35 eyes with exfoliation syndrome or glaucoma, were studied immunohistochemically with monoclonal antibody (MAb) CS-56 to CSPG, MAb TN2 to tenascin, and MAbs HNK-I and VC1.1 to the HNK-1 epitope. Additionally, four frozen lens capsules with exfoliation material were studied by indirect immunofluoresence. • Results: A population of dendritic cells in the inner connective tissue layer of the ciliary body and exfoliation material were immunoreactive with antibodies to the HNK-1 epitope, but no labelling for CSPG and tenascin was seen in them, including frozen sections. The inner surface of the nonpigmented ciliary epithelium was reactive for the HNK-1 epitope, and at the ora serrata also for CSPG. In some eyes with glaucoma, immunoreaction for CSPG and tenascin was seen beneath the epithelium and endothelium of the cornea. The nerve fibre layer of the retina was labelled for tenascin. In the sclera, all antibodies labelled the ground substance, and in some large blood vessels immunoreaction for CSPG and tenascin was seen subendothelially. • Conclusion: Apart from the sclera, the distribution of CSPG and tenascin was different from that of the HNK-1 epitope, suggesting that this carbohydrate epitope may not be borne by these molecules in the human ciliary body.
Similar content being viewed by others
References
Abo T, Balch CM (1981) A differentiation antigen of human NK and K cells identified by a monoclonal antibody (HNK-1). J Immunol 127:1024–1029
Aoyama N, Kikawada R, Yamashina SY (1993) Immunohistochemical study on the development of the rat heart conduction system using anti-Leu-7 antibody. Arch Histol Cytol 56:303–315
Arimatsu Y, Naegele JR, Barnstable CJ (1987) Molecular markers of neuronal subpopulations in layers 4, 5, and 6 of cat primary visual cortex. J Neurosci 7:1250–1263
Avnur Z, Geiger B (1984) Immunocytochemical localization of native chondroitin sulfate in tissues and cultured cells using specific monoclonal antibody. Cell 38:811–822
Baba H (1983) Histochemical and polarization optical investigation for glycosaminoglycans in exfoliation syndrome. Graefe's Arch Clin Exp Ophthalmol 221:106–109
Bollensen E, Schachner M (1987) The peripheral myelin glycoprotein Po expresses the L2/HNK-1 and L3 carbohydrate structures shared by neural adhesion molecules. Neurosci Lett 82:77–82
Bon S, Méflah K, Musset F, Grassi J, Massoulié J (1987) An immunoglobulin M monoclonal antibody, recognizing a subset of acetylcholinesterase molecules from electric organs of Electrophorus and Torpedo, belongs to the HNK-1 anti-carbohydrate family. J Neurochem 49:1720–1731
Chou DKH, Ilyas AA, Evans JE, Costello C, Quarles RH, Jungalwala FB (1986) Structure of sulfated glucuronyl glycolipids in the nervous system reacting with HNK-1 antibody and some IgM paraproteins in neuropathy. J Biol Chem 261:11717–11725
Daugaard S, Strange L, Schiødt T (1991) Immunohistochemical staining for chondroitin sulphate and keratan sulphate. An evaluation of two monoclonal antibodies. Histochemistry 95:585–589
Faissner A, Kruse J, Chiquet-Ehrismann R, Mackie E (1988) The high-molecular-weight J1 glycoproteins are immunochemically related to tenascin. Differentiation 37:104–114
Grumet M, Hoffman S, Crossin KL, Edelman GM (1985) Cytotactin, an extracellular matrix protein of neural and nonneural tissues that mediates glia-neuron interaction. Proc Nail Acad Sci USA 82:8075–8079
Hageman GS, Johnson LV (1987) Chondroitin 6-sulfate glycosaminoglycan is a major constituent of primate cone photoreceptor matrix sheaths. Curr Eye Res 6:639–646
Hoffman S, Edelman GM (1987) A proteoglycan with HNK-1 antigenic determinants is a neuron-associated ligand for cytotactin. Proc Natl Acad Sci USA 84:2523–2527
Hogan MJ, Alvarado JA, Weddel JE (1971) Histology of the human eye. An atlas and textbook. Saunders, Philadelphia, pp 260–319
Kitada S, Shapourifar-Tehrani S, Smyth RJ, Lee DA (1991) Characterization of human and rabbit pigmented and nonpigmented ciliary body epithelium. Curr Eye Res 10:409–415
Kivelä T (1986) Expression of the HNK-1 carbohydrate epitope in human retina and retinoblastoma. An immunohistochemical study with the anti-Leu-7 monoclonal antibody. Virchows Arch [A] 410:139–146
Koukoulis GK, Gould VE, Bhattacharyya A, Gould JE, Howeedy AA, Virtanen I (1991) Tenascin in normal, reactive, hyperplastic, and neoplastic tissues: biologic and pathologic implications. Hum Pathol 22:636–643
Kruse J, Mailhammer R, Wernecke H, Faissner A, Sommer I, Goridis C, Schachner M (1984) Neural cell adhesion molecules and myelin-associated glycoprotein share a common carbohydrate moiety recognized by monoclonal antibodies L2 and HNK-1. Nature 311:153–155
Kruse J, Keilhauer G, Faissner A, Timpl R, Schachner, M. (1985) The J1 glycoprotein — a novel nervous system cell adhesion molecule of the L2/ HNK-1 family. Nature 316:146–148
Lallier T, Bronner-Fraser M (1992) α1ß1 Integrin on neural crest cells recognizes some laminin substrata in a Ca2+-independent manner. J Cell Biol 119:1335–1345
Lightner VA, Gumkowski F, Bigner DD, Erickson HP (1989) Tenascin/Hexabrahion in human skin: biochemical identification and localization by light and electron microscopy. J Cell Biol 108:2483–2493
Margolis RK, Ripellino JA, Goossen B, Steinbrich R, Margolis RU (1987) Occurrence of the HNK-1 epitope (3-sulfoglucuronic acid) in PC12 pheochromocytoma cells, chromaffin granule membranes, and chondroitin sulfate proteoglycans. Biochem Biophys Res Commun 145:1142–1148
Marshall GE, Konstas AGP, Abraham S, Lee WR (1992) Extracellular matrix in aged human ciliary body: an immunoelectron microscope study. Invest Ophthalmol Vis Sci 33:2546–2560
McGarry RC, Helfand SL, Quarles RH, Roder JC (1983) Recognition of myelin-associated glycoprotein by the monoclonal antibody HNK-1. Nature 306:376–378
Nordlander RH (1993) Cellular and subcellular distribution of HNK-1 immunoreactivity in the neural tube of Xenopus. J Comp Neurol 335:538–551
Perentes E, Herbort CP, Rubinstein LJ, Herman MM, Uffer S, Donoso LA, Collins VP (1987) Immunohistochemical characterization of human retinoblastomas in situ with multiple markers. Am J Ophthalmol 103:647–658
Perez RG, Halfter W (1993) Tenascin in the developing chick visual system: distribution and potential role as a modulator of retinal axon growth. Dev Biol 156:278–292
Pesheva P, Horwitz AF, Schachner M (1987) Integrin, the cell surface receptor for fibronectin and laminin, expresses the L2/HNK-1 and L3 carbohydrate structures shared by adhesion molecules. Neurosci Lett 83:303–306
Rittig M, Lütjen-Drecoll E, Rauterberg J, Jander R, Mollenhauer J (1990) Type-VI collagen in the human iris and ciliary body. Cell Tissue Res 259:305–312
Schlötzer-Schrehardt U, Dörfler S, Naumann GOH (1992) Immunohistochemical localization of basement membrane components in pseudoexfoliation material of the lens capsule. Curr Eye Res 11:343–355
Schlötzer-Schrehardt U, Küchle M, Dörfler S, Naumann GOH (1993) Pseudoexfoliative material in the eyelid skin of pseudoexfoliation-suspect patients: a clinico-histopathological correlation. Ger J Ophthalmol 2:51–60
Tawara A, Varner HH, Hollyfield JG (1989) Distribution and characterization of sulfated proteoglycans in the human trabecular tissue. Invest Ophthalmol Vis Sci 30:2215–2231
Tervo K, Tervo T, van Setten GB, Tarkkanen A, Virtanen I (1989) Demonstration of tenascin-like immunoreactivity in rabbit corneal wounds. Acta Ophthalmol 67:347–350
Tervo T, van Setten GB, Lehto I, Tervo K, Tarkkanen A, Virtanen I (1990) Immunohistochemical demonstration of tenascin in the normal human limbus with special reference to tra beculectomy. Ophthalmic Res 22:128–133
Uusitalo M, Kivela T, Tarkkanen A (1993) Identification of a novel element in the human eye: the inner connective tissue layer of the ciliary body characterized with antibodies to the HNK-1 epitope. Invest Ophthalmol Vis Sci 34:2372–2381
Uusitalo M, Kivelä T, Tarkkanen A (1993) Immunoreactivity of exfoliation material for the cell adhesion-related HNK-1 carbohydrate epitope. Arch Ophthalmol 111:1419–1423
Uusitalo M, Kivela T, Tarkkanen A (1994) The HNK-1 epitope in the inner connective tissue layer of the human ciliary body in exfoliation syndrome and various types of glaucoma. Graefe's Arch Clin Exp Ophthalmol 232:8–15
Zaremba S, Naegele JR, Barnstable CJ, Hockfield S (1990) Neuronal subsets express multiple high-molecular-weight cell-surface glycoconjugates defined by monoclonal antibodies Cat-301 and VCL1. J Neurosci 10:2985–2995
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Uusitalo, M. Immunohistochemical localization of chondroitin sulfate proteoglycan and tenascin in the human eye compared with the HNK-1 epitope. Graefe's Arch Clin Exp Ophthalmol 232, 657–665 (1994). https://doi.org/10.1007/BF00171380
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00171380